Sexual selection with age-dependent mutation

I recently got the opportunity to give a talk at both UNC and Eastern Carolina University on my current research project. The talk is available over at figshare if you’d like to scrutinize the details. I’ll give you some of the background here since the talks have no narration.

For starters I’m interested in males that provide only potential genetic benefits to their offspring; I’m also looking at the model where females are assessing male genetic quality based on a male morphological trait (such as an ornament, weapon or body size). This means that females expect to have offspring that are both more sexy and who survive better when she mates with a highly ornamented male, rather than a less well-ornamented male. The problem in this setting is the “lek paradox,” where eventually a female will do just as good to mate randomly as she would to be choosy, since there will be no genetic variation in ornamentation or condition. Usually in models we use mutation to maintain genetic variation for condition; I think I’ve found that being more specific about the type of mutation gives us a good theory that will resolve the lek paradox (yet again!).

My question specifically deals with the scenario where males all start out with the same trait value and then grow that trait throughout their lives (I call this an age-dependent trait). Females can’t tell who is in good condition when looking just at young males. Several models have shown that age-dependent traits are a good strategy for males with relatively good health. They will have more matings over their lifetimes if they ramp up their signaling over their lifetimes. One particular model showed that if males are in good health, they should delay as long as possible, so as not to incur the wrath of natural selection, until they have had lots of opportunities to mate. Lower condition males should adopt a “hope I die before I get old” strategy and be as sexy as possible, as soon as possible.

The problem with these models is that they assume the full range of strategic variation is present in a particular population. They don’t represent changes over time; they just say what the best strategies are. I showed in a previous model that in a population-genetic simulation an age-dependent trait that starts out small will lead to the evolution of preferences and age-dependent traits. This makes sense from a dynamical point of view because selection is weaker at older ages: since older-aged males are only a small fraction of the population, any genetic variation in those males will not contribute much to the whole pot of variation. Selection can’t do much with genetic variation in older males, hence they are relatively free to be as extravagant as they want.

But what if old, sexy males are carrying mutations in their sperm that females cannot detect? I assumed that males will contribute harmful (deleterious) mutations to their offspring at a rate that is basically their age times a per-age mutation rate. I also assumed that the trait increases linearly. This is not realistic, as a lot of traits grow up to a point and then stop or even decline in old age. However, it gets the point across that young males are similarly sized and old males vary in their traits depending on their condition.

The results I have as of yet show that this process actually ensures continued genetic variation in the overall condition trait. The equilibrium female preference hovers above the equilibrium trait size, ensuring that females will always be going for the older, sexier males that carry mutations in their sperm. Mate choice therefore reinforces the process that keeps genetic variation in the population. I hope this result holds up under further mathematical scrutiny, because it’s a nice surprise.

I have a few snags to work out before I write this up; the feedback I got from the talks was invaluable. A few people had really great ideas, like a female strategy to screen sperm for deleterious mutations, and a research strategy to scan sperm samples for such mutations. Although my first reaction was “that’s going to be a lot of work!” my host chimed in that someone actually is doing this already. Wow!

In human mating, there are only two quantities of value females consider in mate choice:

1) Genetic benefits for her offspring (indexed for physical appearance); having a child with older men carries significantly higher risks of birth defects through mutations. And 2) direct benefits (indicated in investment strategies with respect to material resources, and paternal investment). Older husbands far more likely to die, have a shorter life-span, and leave the mother without support so there are significant disadvantages. Let’s see:

1) Regarding to genetic beneficits: Mutations increase with age, by sequencing family trios. Women contribute about 15 de novo mutations, independent of age. Men contribute more (55 on average), and the number increases rapidly with age. The average 20-year old father pass on 25 mutations, while the average 40-year old pass on 65, an increase of about two mutations per year of paternal age.

What do I mean by a modest difference? Assume that population A has an average paternal age of 25: then the average number of new mutations per generation is 50. Assume that population B has an average paternal age of 30: then the average number of new mutations per generation is 60, a 20% increase. It seems that multifactorial disorders that result from impaired brain function, such as autism, schizophrenia, dyslexia and reduced intelligence, are particularly susceptible to the paternal-age effect. This is consistent with the fact that more genes are expressed in the brain than in any other organ, meaning that the fraction of new mutations that will affect its functions is the highest. So, what is the likely consequence of a higher paternal age? Population B will eventually be significantly dumber and crazier than population A.

I would guess that paternal age was not too high for most hunter-gatherers Sapiens. It should have been pretty low in Neanderthals, since they don’t seem to have lived to be very old, probably as a consequence of their high-risk hunting strategy. I would also guess that it can sometimes be considerably higher in post-Neolithic societies with greater inequality of wealth, which often leads to unequal reproduction.

2) Regarding to direct benefits: Age can be indicated as the main factors for physical performance and the levels of physical fitness decrease with age. A more marked decrease in performance is identified soon after 30 years of age and, in some cases (performance stability is observed between 20 and 30 years of age). The third decade of life is indicated as a period of stabilization in lung function that tends to decrease gradually.

This decrease follows an age-related pattern; however, the decrease between 40 and 50 years of age tends to be associated with factors such as increase in body weight, instead of being associated with actual tissue alterations. Regarding the physical fitness variables, a decrease of approximately 10 to 15% in aerobic power is estimated for each decade of life as individuals approach their 3rd decade. (Althoug it seems that the loss can be as little as 5% to 7% per decade in highly trained individuals)

A non-linear decrease in localized muscle resistance in both arm flexions and abdominal exercises at the adult phase has been previously reported and decreases in muscular strength have been reported from over 30 years old.